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Temporal-Prefrontal Bundles in Both Humans and Monkeys

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Temporal-Prefrontal Bundles in Both Humans and Monkeys RESEARCH ARTICLE Dichotomous organization of amygdala/ temporal-prefrontal bundles in both humans and monkeys Davide Folloni1,2*, Jerome Sallet1,2, Alexandre A Khrapitchev3, Nicola Sibson3, Lennart Verhagen1,2,4†, Rogier B Mars2,4† 1Wellcome Centre for Integrative Neuroimaging (WIN),Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom; 2Wellcome Centre for Integrative Neuroimaging (WIN), Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom; 3Department of Oncology, Cancer Research UK and Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford, Oxford, United Kingdom; 4Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands Abstract The interactions of anterior temporal structures, and especially the amygdala, with the prefrontal cortex are pivotal to learning, decision-making, and socio-emotional regulation. A clear anatomical description of the organization and dissociation of fiber bundles linking anterior temporal cortex/amygdala and prefrontal cortex in humans is still lacking. Using diffusion imaging techniques, we reconstructed fiber bundles between these anatomical regions in human and macaque brains. First, by studying macaques, we assessed which aspects of connectivity known from tracer studies could be identified with diffusion imaging. Second, by comparing diffusion imaging results in humans and macaques, we estimated the patterns of fibers coursing between *For correspondence: human amygdala and prefrontal cortex and compared them with those in the monkey. In posterior [email protected] prefrontal cortex, we observed a prominent and well-preserved bifurcation of bundles into †These authors contributed primarily two fiber systems—an amygdalofugal path and an uncinate path—in both species. This equally to this work dissociation fades away in more rostral prefrontal regions. DOI: https://doi.org/10.7554/eLife.47175.001 Competing interests: The authors declare that no competing interests exist. Funding: See page 17 Introduction Received: 26 March 2019 The neural circuits centered on the amygdala and temporal lobe on the one hand and the prefrontal Accepted: 12 September 2019 cortex on the other are crucial in a variety of complex behaviors, including reward-based learning Published: 05 November 2019 and decision-making (De Martino et al., 2006; Hunt and Hayden, 2017; Morrison and Salzman, 2010; Murray and Wise, 2010; Rudebeck and Murray, 2014; Rushworth et al., 2011), Reviewing editor: Sarah Heilbronner, University of and emotional and social behavior (Klu¨ver and Bucy, 1937; Weiskrantz, 1956; Noonan et al., Minnesota, United States 2014; Volman et al., 2011; Whalen et al., 1998). Recent models increasingly emphasize how the amygdala, a complex subcortical area located in the medial bank of the anterior temporal lobe, and Copyright Folloni et al. This the prefrontal cortex (PFC) do not support isolated computations but instead have complementary article is distributed under the roles in these processes (Munuera et al., 2018; Saez et al., 2015; Murray and Wise, 2010). Similar terms of the Creative Commons Attribution License, which computational divisions of labor have been proposed for the anterior temporal association cortex permits unrestricted use and and the prefrontal cortex (Freedman et al., 2003). redistribution provided that the Understanding these computational roles requires an understanding of the anatomy of the brain original author and source are systems that are involved (Marr, 1982). Specifically, we want to understand the principles of connec- credited. tivity between amygdala/anterior temporal systems and prefrontal systems, in order to better Folloni et al. eLife 2019;8:e47175. DOI: https://doi.org/10.7554/eLife.47175 1 of 23 Research article Neuroscience comprehend how information can flow between the various nodes of these networks. Such princi- ples, for instance, are evident in early models by Carmichael and Price (1995) that argue for a mostly dichotomous organization of circuits stretching across temporal and frontal lobes. This line of work, however, has mostly been based on invasive tracer studies that measure area-to-area connec- tions with high spatial accuracy. These approaches are not available for in-vivo human studies. Recent work on diffusion MRI tractography, the only available method to establish structural connec- tivity in-vivo, has demonstrated that using this approach to reconstruct area-to-area connections has many pitfalls (Maier-Hein et al., 2017; Reveley et al., 2017). A more feasible strategy is to reconstruct fiber bundles (Mars et al., 2016a; Thiebaut de Schotten et al., 2011). By seeding in the reliably identifiable white matter, it becomes possible to isolate the core of fiber bundles and then follow their trajectory towards the gray matter in both directions. Although this technique has the potential to elucidate principles of connectivity between systems, it relies on a different philosophy than the invasive tracer studies, making it difficult to draw firm comparative conclusion between results obtained using the two techniques. Therefore, we here apply this technique first in the macaque monkey, for which tracer results are available and thus comparison of the results of the two techniques is possible, and then to the human. White matter dissections and tract-tracing studies in non-human primates have shown that ante- rior temporal regions, including amygdala, and the frontal lobe have widespread reciprocal connec- tions (Aggleton et al., 2015; Barbas et al., 2011; Barbas and De Olmos, 1990; Ghashghaei et al., 2007; Ghashghaei and Barbas, 2002; Price, 2003; Timbie and Barbas, 2014). Two primary pathways are known to connect anterior temporal regions including the amygdala and the frontal lobe: a major association fiber pathway, the uncinate fascicle (UF) (Amaral and Price, 1984; De´jerine, 1895; Klingler and Gloor, 1960; Kuypers et al., 1965; Nauta, 1961; Thiebaut de Schot- ten et al., 2012; Yeterian et al., 2012), and a limbic-cortical ventral amygdalofugal pathway (from here on also referred simply to as the amygdalofugal pathway, AmF) (Aggleton et al., 1980; Bachevalier et al., 1985; Lehman et al., 2011; Nauta, 1961; Nieuwenhuys et al., 2008; Russchen et al., 1985). To date, the AmF has not been described in great detail in the primate brain in-vivo (Carmichael and Price, 1995; Croxson et al., 2005) and is often omitted from human studies of circuits for social-emotional behavior and decision making (Alm et al., 2015; Ameis and Catani, 2015), even though its role in cognitive and emotional processes in animals is critical (Bachevalier et al., 1985; de Guglielmo et al., 2019). Therefore, we focus our investigation on the translatability of knowledge of macaque amygdala/anterior temporal-prefrontal fiber bundles to the human brain along these two tracts. We used high-resolution diffusion MRI data in the macaque to ascertain the degree to which the diffusion MRI tractography approach identified aspects of amygdala/anterior temporal-prefrontal connectivity known from previous macaque studies. This demonstrated that the core bundles of the AmF perforate the porous substantia innominata in the basal forebrain. In this inhomogeneous tis- sue, the fractional anisotropy index is not fully informative of tract integrity. This could lead to false negatives in deterministic tractography, but the probabilistic tractography approach that we employ here demonstrates a distribution of streamlines running through this area. Accordingly, here we have adopted a probabilistic approach to tractography that is strongly informed by prior anatomical knowledge to reconstruct this tract in a manner similar to that used in previous tract tracing studies. Using this approach, we were able to robustlydefine and to dissociate a medial amygdalofugal pathway and an orbital uncinate tract in both the macaque and human brain. Together, these path- ways form a larger constellation of amygdala/anterior temporal-prefrontal circuits, but each with a distinct connectional profile interfacing with a unique set of brain regions. While the amygdalofugal pathway predominantly ran in the white matter exntending between the amygdala, nucleus accum- bens, and subgenual cingulate, ventromedial, and frontopolar regions in ventral PFC, the uncinate pathway primarily coursed in the white matter adjacent to anterior temporal regions, including the amygdala, lateral orbital areas and frontopolar cortex. The relationship and structure of these tracts is preserved across primate species, supporting the translation of insights from non-human primate anatomy to inform our understanding of the human brain. Folloni et al. eLife 2019;8:e47175. DOI: https://doi.org/10.7554/eLife.47175 2 of 23 Research article Neuroscience Results Our goal was to reconstruct the anatomical organization of the amgydalofugal and uncinate bundles in white matter (WM) within amygdala/anterior temporal regions (ATR) and prefrontal territory. In particular, we were interested in assessing the course of these pathways towards the prefrontal cor- tex and their interaction with a wide range of prefrontal regions of interest. Given the difficulty of reconstructing these pathways, we employed the following strategy. First, we reconstructed the tracts in the macaque monkey brain, so that they can be compared to known
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